A vocalization-processing network in marmosets

Jafari, Azadeh; Dureux, Audrey; Zanini, Alessandro; Menon, Ravi S.; Gilbert, Kyle M.; Everling, Stefan

doi:10.1016/j.celrep.2023.112526

Cited by 17 publications

(31 citation statements)

References 67 publications

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“…Lastly, the implanted cranial window used in the current study only covers the auditory cortex including core, belt, and parabelt regions 39 . The vocalization-specific regions in macaques 16 and marmosets 17,40 found previously using fMRI were located in the anterior temporal lobe, which is outside the regions within the cranial window. We expect that there is another voice patch in the anterior temporal lobe.…”

Section: The Existence Of Voice Patches For Processing Species-specif...mentioning

confidence: 69%

Voice patches in the marmoset auditory cortex revealed by wide-field calcium imaging

Zhang,

Song,

Guo

et al. 2024

Preprint

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Species-specific vocalizations are behaviorally critical sounds. Similar to faces, species-specific vocalizations are important for the survival and social interactions of both humans and vocal animals. Face patches have been found in the brains of both human and non-human primates. In humans, a voice patch system has been identified on the lateral superior temporal gurus (STG) that is selective to human voices over other sounds. In non-human primates, while vocalization-selective regions were found on the rostral portion of the temporal lobe outside of the auditory cortex in both macaques and marmosets using functional magnetic resonance imaging (fMRI), it is yet clear whether vocalization-selective regions are present in the auditory cortex. Using wide-field calcium imaging, a technique with both high temporal and high spatial resolution, we discovered two voice patches in the marmoset auditory cortex that preferentially respond to marmoset vocalizations over other sounds and carry call types and identity information. One patch is located on the posterior primary auditory cortex (A1), and the other one is located on the anterior non-core region of the auditory cortex. These voice patches are functionally connected and hierarchically organized as shown by latency and selectivity analyses. Our findings reveal the existence of voice patches in the auditory cortex of marmosets and support the notion that similar cortical architectures are adapted for recognizing communication signals for both vocalizations and faces in different primate species.

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Section: The Existence Of Voice Patches For Processing Species-specif...mentioning

confidence: 69%

Voice patches in the marmoset auditory cortex revealed by wide-field calcium imaging

Zhang,

Song,

Guo

et al. 2024

Preprint

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“…found a gradient of vocalization‐specific responses across the rostral–caudal axis of the ACx, with particularly strong responses near the temporal pole (rostral superior temporal gyrus [STG]), comparable to findings in homologous regions in humans and macaques 85–87 . Rather than finding a similar gradient, Jafari et al 88 . showed “voice patches” in awake marmosets, similar to the human voice patch system, 89 consisting of three distinct voice areas in the temporal cortex.…”

Section: Brain Network Underlying Vocal Perceptionmentioning

confidence: 70%

“…In addition to the frontal cortex, the ACx also projects to various subcortical structures, suggesting these areas may also be involved in the processing of vocalizations. Indeed, Jafari et al 88 . report the activation of several subcortical areas in response to hearing vocalizations and suggest these are part of a larger vocal processing network.…”

Section: Brain Network Underlying Vocal Perceptionmentioning

confidence: 99%

“…Both macaque 91 and marmoset 90 frontal lobes contain patches of face‐selective cells, which are integrated with more extensive face processing and voice processing networks 85,88,216–220 . Primates match the identity of an individual across their face and voice, 104,221 though data on how these social signals are integrated for social recognition at the neural level are only beginning to emerge 222 .…”

Section: Vocal Communication In the Natural Worldmentioning

confidence: 99%

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The neurobiology of vocal communication in marmosets

Grijseels,

Prendergast,

Gorman

et al. 2023

Annals of the New York Academy of Sciences

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An increasingly popular animal model for studying the neural basis of social behavior, cognition, and communication is the common marmoset (Callithrix jacchus). Interest in this New World primate across neuroscience is now being driven by their proclivity for prosociality across their repertoire, high volubility, and rapid development, as well as their amenability to naturalistic testing paradigms and freely moving neural recording and imaging technologies. The complement of these characteristics set marmosets up to be a powerful model of the primate social brain in the years to come. Here, we focus on vocal communication because it is the area that has both made the most progress and illustrates the prodigious potential of this species. We review the current state of the field with a focus on the various brain areas and networks involved in vocal perception and production, comparing the findings from marmosets to other animals, including humans.

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“…fMRI in marmosets has also been improved by the development of optimized hardware, such as the radiofrequency coil (Gilbert et al, 2023; Papoti et al, 2013) and optimized marmoset holders and head-fixation chambers to conduct fully awake MRI (Liu et al, 2013; Schaeffer et al, 2019a). In such environments, a variety of task-based assessments have been established to study visual (Cléry et al, 2020; Hung et al, 2015a, b; Schaeffer et al, 2019b; Schaeffer et al, 2020b), auditory (Jafari et al, 2023; Sadagopan et al, 2015; Toarmino et al, 2017), olfactory (Ferris et al, 2001; Ferris et al, 2004), and tactile processing. Furthermore, brain activity in the resting state has been thoroughly investigated (Belcher et al, 2016; Belcher et al, 2013), and a unique feature of the default mode network in marmosets has been demonstrated (Liu et al, 2019).…”

Section: Introductionmentioning

confidence: 99%

Development of a non-invasive novel individual marmoset holder for evaluation by awake functional magnetic resonance brain imaging

Seki,

Yurimoto,

Kamioka

et al. 2023

Preprint

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BackgroundAlthough functional MRI (fMRI) in awake marmosets (Callithrix jacchus) is fascinating for functional brain mapping and evaluation of brain disease models, it is difficult to launch awake fMRI on scanners with less than 15 cm of bore size. A universal marmoset holder for the small-bore size MRI was designed, and evaluated whether this holder could conduct auditory stimulation fMRI in the awake state.New MethodThe marmoset holder was designed with an outer diameter of 71.9 mm. A holder was designed to allow adjustment according to the individual head shape, enabling to use the holder universally. An awake fMRI study of auditory response was conducted to evaluate the practicality of the new holder. Whole-brain activation was investigated when marmosets heard the marmoset social communication “phee call,” an artificial tone sound, music (bossa nova), and reversed of those.ResultsThe prefrontal cortex was significantly activated in response to phee calls, whereas only the auditory cortex was activated in response to pure tones. In response to bossa nova, the marmoset’s visual and auditory cortices were activated. In contrast, the auditory response was decreased when marmosets heard phee calls and bossa nova music played backward. Their stimulus-specific responses indicated they perceived and differentiated sound characteristics in the fMRI environment.Comparison with Existing MethodsA holder does not require surgical intervention or custom-made helmet to minimize head movement in small space.ConclusionOur newly developed holder made it possible to perform longitudinal fMRI experiments on multiple marmosets in a less invasive manner.HighlightWe designed a universal marmoset holder for the optimization of small-bore size MRI. We aimed to evaluate whether the data acquired by fMRI with this holder indicated that awake marmosets were likely to recognize sounds during fMRI and whether the brain activity shown as fMRI signals reflected the characteristics of each sound.After the acclimatization of the marmosets to the holder, an awake fMRI study was conducted to evaluate the practicality of the new holder and successfully acquired the auditory responses to the set of sound stimuli.Our newly developed holder does not require surgical intervention to minimize head movement, which allows for less invasive fMRI experiments and makes it easier to conduct longitudinal fMRI for multiple marmosets.

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A vocalization-processing network in marmosets

Cited by 17 publications

References 67 publications

Voice patches in the marmoset auditory cortex revealed by wide-field calcium imaging

Voice patches in the marmoset auditory cortex revealed by wide-field calcium imaging

The neurobiology of vocal communication in marmosets

Development of a non-invasive novel individual marmoset holder for evaluation by awake functional magnetic resonance brain imaging

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